Wings, horns, and butterfly eyespots: how do complex traits evolve?

Abstract

Do novel complex traits evolve when pre-existent complex developmental networks are recruited into new places in the body? Here we look closely at the genomic fingerprints that are produced as a result of gene network co-option.

Figure 1. Similar Gene Expression in Various Non-Homologous Structures

The transcription factor Distal-less (Dll) is expressed (A) in the horn primordium of the African dung beetle, Onthophagus nigriventris(modified from [9]); (B) in the eyespot focus of the squinting bush brown butterfly, Bicyclus anynana (modified from [40]); and (C) in the leg imaginal disc of the fruit fly, D. melanogaster (modified from [41]). The transcription factor Spalt (Sal) is expressed (D) in the antenna imaginal disc of D. melanogaster (modified from [42]); and (E) in the eyespot field of B. anynana pupal wings (modified from [12]).

Figure 2. Hypothetical Illustration of Gene Network Co-Option and De Novo Network Evolution

(A) Modular gene network where gene X, at the top of a regulatory network, directs expression of gene Y, which in turn directs expression of gene Z. All these genes are expressed in the tip of an appendage (e.g., leg) depicted on the right. (B) The modular gene network is co-opted into a new tissue by the evolution of a novel CRE in gene X. The Y and Z genes, which only receive inputs from X and Y genes, respectively, are also turned on in the new tissue (e.g., eyespot centers in a butterfly larval wing). The CREs of the Y and Z genes now have a dual function in directing gene expression in two separate developmental contexts, e.g., they are pleiotropic. (C) De novo network evolution where elements of the same non-modular gene network, X, Y, and Z, each evolve a separate CRE that drives gene expression in the novel developmental context.

Figure 3. Examples of Pleiotropic CREs

A schematic representation of putatively pleiotropic CREs is shown for: (A) The spalt (sal and salr) gene complex; (B) spineless (ss); (C) yellow (y); (D) odd-skipped (odd). Gene orientation is marked by arrows. Ovals show approximate position of CREs surrounding the protein-coding genes. Checkmarks of tissue/organs above CREs represent the multiple domains of gene expression driven by the same CRE. Modified from [24,26–28]. The multiple CREs that drive gene expression in the same tissue or organ mostly drive gene expression in distinct cell populations. Abbreviations: CNS, central nervous system; PNS, peripheral nervous system.